# data[].attributes.body
The ability to perceive, interpret, and respond to visual stimuli from the surrounding environment. Vision is 'The process by which light reflected from objects in the environment is transformed into a neural signal that allows for perception, recognition, and action" (Goldstein & Brockmole, 2016). (Sensation and Perception, 10th ed).

E Bruce Goldstein and Brockmole, J.R. (2017). Sensation and perception. 10th ed. Cengage Learning.

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"The ability to extract relevant visual cues from the environment and use them to make accurate and timely motor responses" (Abernethy & Wood 2001) (Journal of Sports Sciences, 19(3), 203-222). Highlights the role vision plays in sports like football.

Abernethy, B. and Wood, J.M. (2001). Do generalized visual training programmes for sport really work? An experimental investigation. Journal of Sports Sciences, 19(3), pp.203–222. doi:https://doi.org/10.1080/026404101750095376.

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Repetitive football heading has been linked to both short-term and long-term impairments in visual function, including changes in visual tracking, depth perception, and ocular-motor control.

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Visual Tracking & Eye Movement Dysfunction

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Visual Tracking & Eye Movement Dysfunction

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Soccer heading leads to temporary impairments in visual tracking and saccadic eye movement, affecting a player's ability to follow a moving object (Caccese et al. 2018). (American Journal of Sports Medicine, 46(14), 3465-3473).

Repeated head impacts can alter ocular-motor control, leading to slower reaction times and difficulties in gaze stabilisation (Rutherford et al. 2009) (British Journal of Sports Medicine, 43(10), 829-834).

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Frequent heading affects binocular vision, reducing depth perception, which is crucial for accurately judging distance during play (Gysland et al. 2012) (Clinical Journal of Sport Medicine, 22(1), 45-50).

MRI scans showed that white matter changes in the temporo-occipital region of the brain, caused by frequent heading, may contribute to deficits in spatial awareness and visual perception (Lipton et al. 2013) (Radiology, 268(3), 850-857).

The temporo-occipital region

The temporo-occipital region is an area of the brain involved in visual processing, object recognition, and spatial awareness.

The occipital lobe houses the primary visual cortex. It processes incoming visual stimuli. The temporal lobe recognises and interprets these images (Grill-Spector & Malach, 2004, Nature Reviews Neuroscience).

Spatial Awareness - Helps integrate visual information with movement, which is essential for depth perception and coordinating motor responses (Goodale & Milner, 1992, Trends in Neurosciences).

Football heading affecting the TOR

White matter changes - football heading associated with micro-structural alterations in the temporo-occipital white matter impacting visual processing and spatial awareness. (Lipton)

Reduced visual performance - short-term impairments in visual tracking and ocular-motor control linked to dysfunction in this region. (Caccese)

Cognitive and Visual Deficits - delayed reaction times, depth-perception issues, and visual recognition difficulties associated with damage to this area. All are crucial for footballers (Gysland).

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The mental processes involved in acquiring, processing, and using information. Includes functions such as memory, attention, problem-solving, and decision-making.

Neuroscientist definition: "Cognition encompasses mental functions including perception, memory, attention, and executive control, which enable goal-directed behaviour" (Miller & Cuttler, 2003, Trends in Cognitive Sciences).

Sports Science Definition: "In sport, cognition involves the ability to process visual, spatial, and tactical information to make rapid and effective decisions" (Vestberg, et al., 2012 PLOS ONE).

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Football heading can impact cognition both short-term (acute) and (cumulative) through repeated sub-concussive impacts, which may disrupt brain fuction.

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Memory and Learning Impairments

Found that 20 headers in a single session led to tmeporary memory and attention deficits lasting up to 24 hours (Di Virgilio et al. 2016) (EBioMedicine, 13, 66-71).

Executive Function Deficits (Decision-Making & Cognitive Control)

Showed that professional footballers with a history of frequent heading performed worse on executive function tests compared to non-players (Master et al. 1999)

Reported that heading impairs the ability to switch tasks and process complex information, which is essential for quick decision-making in football (Rodrigues et al 2016).

Attention and Processing Speed Reduction

Found that youth players who engaged in repetitive heading had slower reaction times and decreased attention span immediately after heading sessions (Press et al. 2017).

Repeated heading may contribute to long-term cognitive slowing, resembling early signs of neurodegeneration (Stewart et al 2016).

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The Role of the Prefrontal Cortex (PC) in Cognition & Heading

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The Role of the Prefrontal Cortex (PC) in Cognition & Heading

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The PC is responsible for decision-making, attention control, and working memory (Miller & Cohen, 2001, Annual Review of Neurosciences).

Neuroimaging studies suggest that football heading may lead to functional disruptions in the PC, affecting cognitive control and response inhibition (Lipton et al, 2013).

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Perception is the process of interpreting sensory information to understand and interact with the environment. It allows individuals to recognise objects, judge distance, and coordinate movements effectively.

Neuroscientific Definition: "Perception is the organisation, identification, and interpretation of sensory information, and interpretation of sensory information in order to represent and understand the environment" (Goldstein and Brockmole, 2016, Sensation and Perception).

Sports Science Definition: "Perception in sport involves the ability to rapidly extract relevant sensory cues from the environment to guide motor responses and decision-making" (Abernethy & Wood, 2001, Journal of Sports Sciences 19(3), 203-222).

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Football heading can disrupt sensory processing, particularly in spatial awareness, depth perception, and motion tracking.

# data[].attributes.headline
Spatial Awareness & Motion Perception Impairments

# data[].attributes.subject
Spatial Awareness & Motion Perception Impairments

# data[].attributes.body
Reported that soccer players who frequently head the ball showed reduced accuracy in tracking moving objects, potentially affecting their ability to judge the speed and trajectory of the ball (Rodrigues et al. 2016) (Frontiers in Neurology, 7, 38).

# data[].attributes.body
Found that repetitive heading leads to temporary impairments in binocular vision, which affects depth perception (Gysland et al. 2012) (Clinical Journal of Sport Medicine, 22(1), 45-50).

Showed that players who headed the ball multiple times had delayed visual responses, making it harder to judge distances accurately (Caccese et al. 2018) (American Journal of Sports Medicine, 46(14), 3465-3473).

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Vestibular Dysfunction & Balance Perception Issues

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Vestibular Dysfunction & Balance Perception Issues

# data[].attributes.body
Demonstrated that heading can disrupt vestibular function, leading to temporary balance and postural control issues (Haran et al. 2013) (International Journal of Sports Medicine, 34(4), 350-354).

Found that youth players exhibited short-term dizziness and instability post-heading, likely due to disruptions in sensory integration (Press et al. 2017) (Medicine & Science in Sports & Exercise, 49(9), 1899-1905).

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The Role of Occipital and Parietal Lobes in Perception & Heading 

# data[].attributes.subject
The Role of Occipital and Parietal Lobes in Perception & Heading 

# data[].attributes.body
The occipital lobe processes visual stimuli, while parietal lobe integrates spatial information and movement coordination (Goodale & Milner, 1992, Trends in Neurosciences).

Research suggests that repeated impacts from heading may impair the functional connectivity between these areas, leading to deficits in visual motion tracking and spatial judgement (Lipton et al., 2013).

# data[].attributes.attachment_link.title
Immediate effects of an acute bout of repeated soccer heading on cognitive performance

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Purpose: There isgrowing concern surrounding the harmful effects of soccer heading on cognitive function. The present study aims to examine the immediate effects of heading.Methods: 30 recreational…

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Frontiers | Effects of Soccer Heading on Brain Structure and Function

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Soccer is the most popular sport in the world, with more than 265 million players worldwide, including professional and amateur ones. Soccer is unique in com…

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The King-Devick test as a determinant of head trauma and concussion in boxers and MMA fighters

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Sports-related concussion has received increasing attention as a cause of short- and long-term neurologic symptoms among athletes. The King-Devick (K-D) test is based on measurement of the speed of rapid number naming (reading aloud single-digit…

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Evidence for Acute Electrophysiological and Cognitive Changes Following Routine Soccer Heading - PubMed

# data[].attributes.attachment_link.description
Sub-concussive head impacts routine in soccer heading are associated with immediate, measurable electrophysiological and cognitive impairments. Although these changes in brain function were transient, these effects may signal direct consequences of routine soccer heading on (long-term) brain health …

# data[].attributes.body
Concussions - physical and cognitive symptoms that can be observed by others and/or self-reported by the player themselves.

Sub-concussions - a silent injury and meaning they are unnoticed and undetected by the player and those around them

# data[].attributes.attachment_link.title
Headers and concussions in elite female and male football: a pilot study

# data[].attributes.attachment_link.description
Heading is a risk factor for neurogenerative disease in football. However, the exposure to heading in elite football training is understudied. The primary purpose of this study was to determine the exposure to headers in elite men’s and women’s…

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Soccer heading immediately alters brain function and brain-muscle communication

# data[].attributes.attachment_link.description
There is growing evidence of a link between repetitive soccer heading and the increased incidence of neurodegenerative disease. Even a short bout of soccer heading has been shown to impair cognitive performance and disrupt movement control. However,…

# data[].attributes.body
Definition. Cognitive function is a broad term that refers to mental processes involved in the acquisition of knowledge, manipulation of information, and reasoning. Cognitive functions include the domains of perception, memory, learning, attention, decision making, and language abilities.

Kiely, K.M. (2014). Cognitive Function. In: Michalos, A.C. (eds) Encyclopedia of Quality of Life and Well-Being Research. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0753-5_426

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Chronic traumatic encephalopathy (CTE) is a brain condition thought to be linked to repeated head injuries and blows to the head. It slowly gets worse over time and leads to dementia, but the right help and support can manage the symptoms.

# data[].attributes.attachment_link.title
The spectrum of disease in chronic traumatic encephalopathy - PubMed

# data[].attributes.attachment_link.description
Chronic traumatic encephalopathy is a progressive tauopathy that occurs as a consequence of repetitive mild traumatic brain injury. We analysed post-mortem brains obtained from a cohort of 85 subjects with histories of repetitive mild traumatic brain injury and found evidence of chronic traumatic en …

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Systematic review and meta-analysis of the effects of football heading - PubMed

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We provide the first meta-analytical review of football heading effects aggregated from multiple studies and extended findings from a recent systematic review of the effects of football heading. Our analysis indicates no overall effect for heading a football on adverse outcomes.

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Microsaccades are the largest and fastest of the fixational eye movements, which are involuntary eye movements produced during attempted visual fixation.

https://www.sciencedirect.com/topics/neuroscience/microsaccade

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Microsaccades and interest areas during free-viewing sport task - PubMed

# data[].attributes.attachment_link.description
Microsaccades are important fixation eye movements for visual scene perception. Compared to novices, athletes make fewer fixations of longer duration toward limited interest areas crucial for action prediction. Thus, our aim was to study the microsaccade features during those fixations. Gaze behavio …

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Heading in football: a systematic review of descriptors, definitions, and reporting methods used in heading incidence studies

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The primary objective of this systematic review was to describe the number and type of heading descriptors used in all published studies which report on heading incidence in football. The secondary…

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Start with a broader context: The introduction begins a little abruptly. Consider opening with a few sentences about the significance of heading in football and how it's an integral part of the sport. You might then introduce the emerging concerns, supported by evidence, around increased risks of neurological issues—such as dementia—in players who frequently head the ball. This will help ease the reader into the topic more naturally.

Structure and flow: At the moment, the content jumps between different effects of heading (e.g., cognitive, visual, saccadic). It would strengthen your argument to first discuss the broader cognitive and motor impacts of heading, then move into effects on vision and perception, and finally focus specifically on microsaccades. This progression will make your argument more cohesive and easier to follow.

Research gap: There's no need to include a separate 'Research Gap' section. Instead, try to weave this into the final part of your introduction. You can use this space to clearly highlight what’s currently unknown or underexplored, and how your project addresses that gap.

Referencing: Lastly, please make sure all your references are primary sources and follow a consistent referencing style throughout. At the moment, there are some inconsistencies that need tidying up.

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Chris Johnson and SoccerXpert contributors

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Coaching Points for Heading; Offensive and Defensive

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Heading is an essential skill for both offensive players attempting to score and defensive players protecting their goal.

# data[].attributes.attachment_link.title
Heading in football: a systematic review of descriptors, definitions, and reporting methods used in heading incidence studies

# data[].attributes.attachment_link.description
The primary objective of this systematic review was to describe the number and type of heading descriptors used in all published studies which report on heading incidence in football. The secondary…

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By Lim Weiyang
MASTER YOUR FOOTBALL TECHNIQUE (8): HEADERS

In the game of soccer, aside from using your legs, the only other body part you can use to generate power, accuracy and distance would be your head. The head is also the highest body part, making it possible to reach the ball quicker than a player just adept at using his feet. As such, mastering heading is very important in becoming a good footballer.

Many teams make long overhead passes, especially during goal kicks as it gets the ball up-field and eliminates the risk of interception. In situations where the ball is still in the air, which team gains possession often boils down to who wins the aerial duel between your receiving player and the opposition. There are football teams that fashion their tactics around this advantage and they play what is termed "direct" football, which you can read up more about underfootball formations.

In this article, we will discuss the methodologies of heading in different scenarios as well as the actual technique used for heading a football.

Defensive headers
For defensive headers, you want to be heading the ball at an angle away from your post and upwards into the air. You should never head downwards unless you are extremely certain that your teammate would receive the ball. To get the ball upwards, use your forehead to make contact with the underside of the football.

The reason why you head upwards is so you buy time and allow your defence to get ready and perhaps even engage in another aerial duel. If you head it downwards, it may go to the feet of your opposition and you will have committed a great injustice to your team. So remember, for defensive headers, head the ball upwards and away from goal.
Offensive headers
If you are in a goal-scoring position such as being within the 6 yard box or penalty box, you will want to direct the ball with your head with power and downwards at goal. To do so, you first need to leap higher than the football and make contact with the top half of the football. The important thing to remember during an offensive header is to keep the ball low and to use power!

1. Where is the ball going to land?

Study the trajectory of the ball and position yourself where the ball will be for you to head.

2. Always make contact with your forehead

Your forehead is the area that will generate the most power and cause the least pain to yourself. Avoid using your scalp as the accuracy will be poor and it has a higher risk of head injury from high impact balls. Engage your neck muscles just before your forehead makes contact with the ball.

3. Open your eyes, close your mouth and clench your teeth

Opening your eyes would ensure you don't crash into opposing or friendly players. It may be hard to get used to at first as its a reflex action to close your eyes upon impact. Closing your mouth and clenching your teeth is extremely important as it prevents you from accidentally biting your tongue or breaking a tooth during a forceful header.
To receive the latest updates on the happenings in the Singapore sports scene, or to find out more about some of the latest programmes on offer at ActiveSG, like our Facebook pagehere. Interested in football and want to hone your skills with the best? Or perhaps you are a parent wishing to expose your child to the beautiful game? If your answer to either of the above is yes, then ActiveSG Football Academy is the place for you to be at. Led by former Singapore international Aleksandar Duric, and five head coaches with experience from the highest level of football in Singapore: Richard Bok, Robin Chitrakar, Hyrizan Jufri, Mohamad Hairil Amin, Isa Halim, and Steven Tan, ActiveSG Football Academy has a holistic football programme designed to build character and impart the right skills while encouraging trainees to pursue their sporting passion with the right attitude. To find out more or sign up for the academy, visit this linkhere.

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An article that provides tips on the right technique to head a football, and the different types of headers used.

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Abstract

Introduction

There is growing concern around the effects of concussion and sub-concussive impacts in sport. Routine game-play in soccer involves intentional and repeated head impacts through ball heading. Although heading is frequently cited as a risk to brain health, little data exist regarding the consequences of this activity. This study aims to assess the immediate outcomes of routine football heading using direct and sensitive measures of brain function.

Methods

Nineteen amateur football players (5 females; age 22 ± 3 y) headed machine-projected soccer balls at standardized speeds, modelling routine soccer practice. The primary outcome measure of corticomotor inhibition measured using transcranial magnetic stimulation, was assessed prior to heading and repeated immediately, 24 h, 48 h and 2 weeks post-heading. Secondary outcome measures were cortical excitability, postural control, and cognitive function.

Results

Immediately following heading an increase in corticomotor inhibition was detected; further to these electrophysiological alterations, measurable reduction memory function were also found. These acute changes appear transient, with values normalizing 24 h post-heading.

Discussion

Sub-concussive head impacts routine in soccer heading are associated with immediate, measurable electrophysiological and cognitive impairments. Although these changes in brain function were transient, these effects may signal direct consequences of routine soccer heading on (long-term) brain health which requires further study.

Keywords: Sports concussion, Transcranial magnetic stimulation, Sub-concussion, Traumatic brain injury

Highlights

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Standard soccer heading results in immediate and measurable alterations in brain function.

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Changes in short and long term memory function and corticomotor inhibition are detectable immediately after soccer heading.

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These changes in brain function after just a single session of heading appear transient.

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These data provide direct evidence of immediate brain functional impairment associated with soccer heading.

Questions have been raised over whether soccer heading might have an effect on a player's brain, with particular worry over the proposed link between brain injury and increased risk of dementia. However, until now there have been no studies of the immediate effects of heading in soccer directly on brain function. This study found that just a single session of heading practice resulted in temporary impairment of short and long term memory function and in electrophysiological function of the brain. Whether these effects remain temporary after repeated soccer heading exposure and their long-term consequences on brain health must now be investigated.

1. Introduction

With increased awareness of immediate and late complications of head injuries in sport, in particular the proposed association between exposure to repetitive concussion and late neurodegenerative disease ( Hay et al., 2016), there have been considerable efforts to reduce risk of injury and better manage concussions when they do arise ( McCrory et al., 2013). Soccer (association football) is acknowledged as the most popular participation sport globally, with routine game-play in soccer involving intentional and repeated head impacts through heading the ball; a skill regularly included in training sessions and from a young age. Therefore, although rates of concussion are relative low in soccer compared to other contact sports such as rugby union or American football ( Pfister et al., 2016), participation rates and the incidence of intentional sub-concussive impacts through heading in training and match play are such that the safety of heading in soccer has been questioned in some quarters ( Patlak and Joy, 2002).

Though accepted as part of routine game-play, emerging evidence suggests exposure to repeated sub-concussive impacts in soccer may be associated with measurable changes in brain structure and function, and perhaps with late neurodegenerative disease. Rotational headers may prove of particular interest as they are often performed in training drills and matches (i.e. corner kicks) and are believed to be more injurious compared to linear accelerations ( Cantu and Hyman, 2012). Imaging studies over the course of a season in active soccer players report evidence of white matter microstructural changes with associated impaired cognition ( Lipton et al., 2013). Further, imaging of former professional soccer players aged 40-65 demonstrates evidence of cortical thinning, again with associated cognitive impairment ( Koerte et al., 2015). Regarding longer term outcomes, recent identification of a form of dementia known as chronic traumatic encephalopathy (CTE) in athletes from a range of contact sports (for review see Smith et al., 2013) including soccer ( Geddes et al., 1999, McKee et al., 2014) has drawn attention to the possibility that head impacts in soccer might be associated with increased risk of neurodegenerative disease.

Nevertheless, despite growing evidence on risks from the cumulative effects of sport-related head impacts and anxieties around the safety of ball-heading, little data exists demonstrating direct consequences of heading on brain function. Transcranial magnetic stimulation (TMS) can be used to assess a variety of indices of function in the brain to muscle pathway ( Goodall et al., 2014). Further, TMS has demonstrated utility in quantifying electrophysiological changes in concussion ( Major et al., 2015). The most consistent TMS marker of concussion (both acutely and longitudinally) appears to be corticomotor inhibition ( Major et al., 2015, Pearce et al., 2015, Miller et al., 2014), expressed by a longer period of electromyographic silence (cortical silent period - cSP), after a motor evoked potential (MEP) is delivered to the primary motor cortex during contraction. Given the apparent high sensitivity to identify alterations in brain function, TMS could potentially be used to detect acute changes in brain function following sub-concussive head impacts. The relative novelty of TMS used in this context makes interpretation in terms clinically meaningful effects difficult, but its appeal is sensitivity in detecting direct brain changes ( De Beaumont et al., 2007). It potentially highlights neurochemical changes that can be used to direct routes of investigation into the effects of sub-concussive impacts on the brain. Therefore, the aim was to study the use of TMS corticomotor inhibition in the lower limbs as primary outcome measure to detect acute changes in brain function from repetitive sub-concussive head impacts simulating routine soccer heading. We hypothesized that there would be a (transient) increase in corticomotor inhibition following a standardized bout of soccer heading, which may be accompanied by measurable changes in other established but less sensitive or less objective indexes of changes to brain function and brain injury as secondary outcome measures such as cognitive tests.

2. Methods

2.1. Approvals and Recruitment

The study was approved by the local Research Ethics Committee and procedures conformed to the guidelines set out by the Declaration of Helsinki. Written informed consent was obtained from all participants, prior to taking part. Twenty-three healthy, amateur football players (5 females; age 22 ± 3 y; weight 72.9 ± 8.3 kg; height 175.4 ± 10.2 cm) were recruited for study via advertisement on university noticeboards and meetings with local football clubs. Participants were excluded from taking part if they presented with any of the following: 1) history of brain injury resulting in loss of consciousness; 2) history of a neurological condition; 3) history of concussion in the 12 months prior to taking part; 4) family history of epilepsy; 5) use of psychoactive recreational or prescription drugs. Data from one participant could not be analyzed and three more participants withdrew from the study for personal reasons. The final cohort included a total of nineteen participants.

2.2. Study Design

Participants were asked to refrain from vigorous physical activity, consuming alcohol and caffeine or smoking for 24 h prior to each study session. Furthermore, participants were required to present to the laboratory fasted where they were provided with a standardized breakfast. At the first experimental session baseline measures for cognitive function, postural control, corticospinal excitability and corticomotor inhibition were recorded in this order; assessments thereafter recorded in the same order at each time point during study. Following baseline testing, participants underwent the heading protocol and then repeated the measures at 4 follow-up time points (taking measures in reverse order from the baseline order, starting with the TMS primary outcome measure); immediately post-heading and at 24 h, 48 h and 14 days following the heading protocol. The decision to include the 48 h follow-up was to assess the transient nature of the effects of heading, and the 14 day follow-up was intended as a time point at which complete "wash out" would have occurred following heading impact. Prior to commencement of study data collection participants attended the laboratory for a familiarization session, during which they completed all outcome measures to acquaint them with the assessment procedures and minimize later learning effects.

2.3. Heading Protocol

The heading protocol consisted of heading a standard football (400 g; 70 cm circumference; 8 psi) projected at a speed of 38·7 ± 2.1 kph from a football delivery device (JUGS sports, Tualatin, USA) positioned 6 m from participants, simulating routine soccer game-play ( Haran et al., 2013, Broglio et al., 2004). Participants were instructed to perform a rotational header, redirecting the football perpendicularly to the initial trajectory, with each session consisting of 20 consecutive head impacts over a 10 min period, replicating typical heading practice. A custom-built accelerometer placed at the back of the participant's head recorded linear g-force of the head during impact. Ball speed was determined based on the participants' perceived ability to head the ball with a minimum speed of 30 kph and maximum speed of 50 kph.

2.4. Transcranial Magnetic Stimulation

Motor evoked potentials (MEPs) were elicited in the rectus femoris of the dominant leg via single pulse TMS and assessed using electromyographic (EMG) recordings (see below). Single magnetic stimuli of 1 ms duration where applied over the contralateral primary motor cortex using a magnetic stimulator (Magstim 200 ² unit, The Magstim Company Ltd., Whitland, UK) and a 110 mm double cone coil. Optimal coil location for generating MEPs was determined by placing the coil over the motor cortex, laterally to the vertex; the area where the largest MEP peak-to-peak amplitudes occurred was identified and marked on the scalp with ink ( Goodall et al., 2009). The active motor threshold for the quadriceps femoris was determined by increasing stimulator output from 10% by 5% increments, while the participant held a 10% maximal voluntary contraction (MVC) isometric contraction until discernible MEPs were visible ( Wilson et al., 1995). Once this individual level was established, subsequent stimulations were delivered at 130% of active motor threshold.

MEPs, alongside all other EMG measures, were recorded with participants sitting with their dominant leg secured to a calibrated load cell of an isokinetic dynamometer (Kin-Com, Chattecx Corp, Chattanooga Group Inc., Tennessee). Knee angle was set at 60° (0° being fully extended limb) and the arm of the dynamometer was set such that the axis of rotation was aligned with the participant's lateral femoral condyle.

To assess the primary outcome measure corticomotor inhibition participants were required to perform maximal knee extensor voluntary contractions (MVCs) of 5 s duration while a single TMS stimulation was delivered over the motor cortex. This was repeated three times with a minute's rest between each contraction, as is common practice. Corticomotor inhibition was quantified as the cortical silent period (cSP) duration, taken from the stimulation artefact to the resumption of discernible, uninterrupted EMG activity from the muscle ( Fig. 1). By measuring cSP at MVC, even though this limits the number of repetitions feasible, we ensure to recruit a motor unit pool large enough to show an effect. Measuring cSP at lower intensity may not be as sensitive since a smaller pool of motor units is recruited, reducing the relative effect size of GABA inhibitory mechanisms on the EMG signal. In turn, making the cSP measurements less sensitive in detecting subtle and transient cortico-spinal changes. During the assessment of secondary outcome measure corticospinal excitability, participants maintained a 20% MVC isometric contraction while 20 single TMS pulses, separated by 6 s, were delivered over the motor cortex. Corticospinal excitability was determined as the average MEP amplitude normalized to the maximal response elicited by motor nerve stimulation (%Mmax, see below). We chose to assess cortical excitability and inhibition in the lower limbs rather than in the upper limbs because of its functional relevance; in soccer, changes in lower limb may be more valid as they relate directly to gait and performance.

2.5. Electromyography and Femoral Nerve Stimulation

Electromyographic activity was recorded using a wireless system (Biopac Systems, Inc. Goleta, CA, USA). Data were sampled at 2 kHz, and filtered using 500 Hz low and 1.0 Hz high band filters. Signals were analyzed offline (Acqknowledge, v3.9.1.6, Biopac Systems, Inc. Goleta, CA, USA). EMG activity was assessed using Ag/AgCl surface electrodes (Vermed, Devon, UK) with an intra-electrode distance of 2 cm positioned over rectus femoris; prior to electrode placement, the area of interest was shaved and abraded as per Surface Electromyography for the Non-Invasive Assessment of Muscles (SENIAM) guidelines. The position of each electrode was marked with permanent ink to ensure consistent placement during subsequent visits.

Peripheral stimulation of the femoral motor nerve was administered using an electrical stimulator (Biopac Systems, Inc.). The stimulation site was identified by locating the femoral artery and placing a self-adhesive surface electrode (cathode) lateral to it, high over the femoral triangle, with the anode on the buttock. Single stimuli were delivered to the muscle while participants maintained a 20% MVC isometric contraction, and the intensity of stimulation was increased until a plateau in twitch amplitude and rectus femoris M-wave (Mmax) occurred. Supramaximal stimulation was delivered by increasing the final stimulator output intensity by a further 30%.

2.6. Cognitive Function

Secondary outcome measure cognitive function was assessed in a quiet room using the Cambridge Neuropsychological Test Automated Battery (CANTAB), a computer based cognitive assessment tool and neuropsychological standard. The following CANTAB tasks were included: Reaction Time (RTI; divided attention); Paired Associate Learning (PAL; long-term memory); Spatial Working Memory (SWM; short-term memory); Attention Switching Task (AST; executive function); and Rapid Visual Processing (RVP; sustained attention).

2.7. Postural Control

Secondary outcome measure postural control was assessed using the Biodex Balance System SD (BBS; Biodex Medical Systems, Inc. New York, USA). Participants stood on a circular dynamic platform and average sway score was determined by measuring the degree of tilt on anterior-posterior and medial-lateral axes during three, 20 s trials (using dedicated Biodex software, v1.08, Biodex Inc.).

2.8. Statistical Analysis

Immediate post-heading responses were analyzed using a paired t-test, comparing measures before and immediately after the heading protocol. Recovery was analyzed for individual growth curves using the SPSS MIXED model with the restricted maximum likelihood method in keeping with standards for analysis of longitudinal data ( Singer and Willett, 2003, Peugh and Enders, 2005). To achieve this, individual curves were analyzed to examine change over time. The following time points were included: immediate post, 24 h post, 48 h post, two weeks post. Data was checked for skewness and kurtosis and three cognitive measures (SWM, PAL, and RVP) and the balance variable were normalized using log transformation. The 95% lower and upper confidence intervals (CIs) were also calculated from difference of the mean values. Effect sizes (ES) were calculated for non-transformed differences using Cohen's d formula and were quantified as follows: 0.2 = small; 0.5 = medium; 0.8 = large. Statistical significance was set at p ≤ 0.05. Each measure was separate in relation to the hypotheses and therefore no correction for multiple comparisons was necessary. Data are expressed as means (± standard deviation) unless otherwise stated. The funding source had no input in the study other than suggesting at the design stage to add a full recovery assessment time-point.

3. Results

Overall, each participant performed 20 headers, achieving a mean force of impact of 13.1 ± 1.9 g ( Table 1), with a coefficient of variance of 18%(± 3%).

3.1. Effect of Heading on Corticomotor Inhibition and Corticospinal Excitability

Immediately after ball heading there was a measurable increase in the primary outcome measure cSP within 74% (14 out of 19) of participants ( Fig. 2). The cSP duration increased from 117.8(± 19.8)ms at baseline to 123.1(± 17.6)ms (t₍₁₈₎ = − 2.11, p = 0.049; ES 0.28), representing an average increase of 5.4(± 4.8)% in cSP duration, compatible with increased corticomotor inhibition. This increase in cSP proved transient with apparent normalization to baseline in subsequent follow-up assessments at 24 h, 48 h and 14 days (F(1,18) = 4.23, p = 0.04) ( Fig. 3). There was a moderate, but not significant, relationship between these acute increases in cSP and g-force on impact with the ball ( r = 0.37, p = 0.07 one-tailed).

To determine the reproducibility of the primary outcome measure the intraclass correlation coefficient (ICC) was calculated between the baseline and the 2 weeks post-measure. ICC for the two measures was 0.764, suggesting excellent agreement ( Cicchetti, 1994). Furthermore, no within-participant differences were found between the two time points using a paired t-test (t₍₁₈₎ = − 0.47, p < 0.63; ES 0.09; CI − 10.36 to 6.53).

No changes were found on the secondary TMS outcome measure corticospinal excitability; MEP amplitude demonstrated no change in the acute phase immediately after ball heading, nor in the follow-up assessment time-points ( Table 2). There was no notable change in knee extensor MVC after heading the ball ( Table 2), suggesting the participants did not experience significant muscular fatigue that might interfere with TMS measurement.

3.2. Altered Cognitive Function Following Heading

Immediately after the heading protocol there was a reduced performance compared to baseline in two CANTAB sub-tasks assessing accuracy on different aspects of memory. Specifically, Spatial Working Memory (SWM) error scores were significantly higher (t₍₁₈₎ = − 2.28, p = 0.03, ES 0.3) immediately after the heading protocol, compatible with impairment in short-term memory ( Fig. 4a). Furthermore, total adjusted error score on the Paired Associated Learning (PAL) task immediately after heading increased by 67% (t₍₁₈₎ = − 3.05, p = 0.007, ES 0.5), compatible with a reduced long-term memory function ( Fig. 4b). These disturbances in short- and long-term memory proved transient, with normalization to baseline performance in SWM (F(1,18) = 10.28, p = 0.002) and PAL (F(1,18) = 11.14, p = 0.002) in the subsequent follow-up assessments at 24 h, 48 h and 14 days ( Table 2).

Heading only significantly affected memory function; the remaining CANTAB tasks assessing aspects of attention and processing speed did not show significant heading-associated decrements compared to baseline assessments ( Table 2). No change was detected on the Rapid Visual Processing task, with RVP A′ scores close to ceiling/maximum, making the measure insensitive to change. There was a marginal improvement on the median corrected latency scores of the executive function Attention Shifting Task (t₍₁₈₎ = 2.52, p = 0.021), possibly due to practice. On the Choice RTI measure there was no effect of heading on decision times (t₍₁₈₎ = 0.69, p = 0.5) ( Table 2).

4. Discussion

Following a standardized session of football heading designed to simulate routine soccer practice our data demonstrate immediate alterations in brain electrophysiological and cognitive function compared to baseline assessments in a cohort of healthy, young soccer players. Specifically, using TMS we found a measurable increase in cortical silent period (cSP) after just 20 consecutive headers. Furthermore, in cognitive assessments, our data demonstrate evidence of decreases in measures of both short- and long-term memory immediately following heading. Notably, in this single exposure paradigm, these alterations in brain corticomotor inhibition and cognitive function appeared short-lived; the effects apparently normalizing in follow-up assessments from 24 h onwards. In contrast to previous studies in athletes and patients with confirmed concussion or mild TBI ( De Beaumont et al., 2007, Chistyakov et al., 2001, Bernabeu et al., 2009, Livingston et al., 2010) these novel observations demonstrate, for the first time, detectable alterations in brain function in footballers exposed to 'routine' head impacts not associated with clinically recognizable brain injury.

The prolonged silent period of neuromuscular recruitment found in this study is a sign of increased inhibition in the motor system and is thought to reflect GABA activity ( Inghilleri et al., 1993, McDonnell et al., 2006) which is the most powerful inhibitor in the motor system. Although the mechanisms behind corticomotor inhibition are not fully understood ( Chen et al., 1999), increased inhibition following repeated sub-concussive head impact may reflect protective mechanisms against minor injury. What is a concern however is that such protective mechanisms could become maladaptive when stimulated repeatedly, as occurs during soccer heading practice. Albeit apparently transient, the acute increases in corticomotor inhibition following football heading could trigger a pathological process damaging brain health through the accumulative effect of sub-concussive head impact. Increased corticomotor inhibition silent period has been found to be associated with pathophysiology in brain damage suggesting a link between functional deficits and hyperactivity of cortical inhibitory interneurons ( Classen et al., 1997). Further study into the dynamic metabolic processes as a direct result of soccer heading is required. When we understand the complex interplay between functional, metabolic, and structural brain changes following repeated sub-concussive head impact, we can establish the link to accumulative and long-term consequences. At present, the current findings at least suggest acute brain changes occur as a direct consequence of soccer heading.

As well as increased corticomotor inhibition, parameters of memory function were altered following the heading protocol, consistent with a recent report of a relationship between memory function and history of heading in soccer ( Lipton et al., 2013). Furthermore, a study of retired Australian Rules footballers found that elite players performed more poorly on the Paired Associate Learning test than amateurs ( Pearce et al., 2014). Practical limitations of cognitive-based tests to detect impairment in athletes are due to reliability: in high performance sports athletes have been recognized to purposely produce low baseline performances on cognitive tests to allow them to avoid removal from play, or to reduce return to play intervals ( Erdal, 2012).

For completeness postural control (balance) was included as a secondary, albeit indirect, outcome measure as concussion has been shown to result in impaired balance ( McCrory et al., 2013, Powers et al., 2014), yet the participants in the current study were able to maintain their balance despite an increased level of corticomotor inhibition. And while one study has shown a decrease in postural control following bouts of soccer heading ( Haran et al., 2013), another study has not ( Broglio et al., 2004); and now our own show no change in postural control.

Secondary TMS outcome measure cortical excitability has previously been shown to decrease following TBI ( De Beaumont et al., 2007, Chistyakov et al., 2001, Bernabeu et al., 2009, Livingston et al., 2010), yet we demonstrated no such change following ball heading. The reason why changes were seen in cortical inhibition and not cortical excitability may be due to the different levels of muscle contractile force applied during recording of the two parameters (20% MVC for excitability vs. 100% MVC for inhibition, see the introduction for its justification). Furthermore, it should be noted that measuring cortical excitability is a less straightforward procedure than corticomotor inhibition as it requires MEP normalization to maximal motor nerve response ( Goodall et al., 2009). Primary outcome measure TMS corticomotor inhibition was thought to be most sensitive to quantifying electrophysiological changes based on a recent systematic review ( Major et al., 2015), and is a direct measure of changes to brain function.

Future work should include a control activity, such as body movement without head impact. However, the current pattern of results leaves little doubt that the changes in brain function were related to head impact rather than physical activity. The force of maximal knee contraction was not reduced after heading, therefore the absence of a physical exercise control group it is highly unlikely to explain the effect on corticomotor inhibition or memory function. Nevertheless, a future extension of this work can focus on the acute effects of heading now that the transience of the effect has been established, and would be well placed to reveal the mechanisms underlying these brain changes through a cross-over design that includes a control activity. Furthermore, because it is likely that sub-concussive impacts are more general in nature (i.e. they do not affect single muscles) future work should assess corticomotor inhibition in a larger number of muscles, possibly encompassing both upper and lower limbs. Further study into the dynamic metabolic processes as a direct result of soccer heading is required. Implementing the use of magnetic resonance spectroscopy in future studies could help determine short-term alterations in GABA and glutamate responses. With regard to changes in GABA, because of the use of single-pulse TMS in this study, we were only able to report on the activity of GABA B, while the use of paired-pulse TMS in future work can distinguish modulation of GABA A and GABA B. Critically, however, the sensitivity of the current primary outcome measure suggests that corticomotor inhibition through future dose-response studies has the potential to provide the evidence-base to guide safe engagement in contact-sports, such as soccer.

5. Conclusion

The current study is the first to show direct evidence for acute changes to corticomotor function and changes to memory function following routine soccer heading. It is furthermore the first study to show that corticomotor inhibition, measured by TMS, is able to detect acute transient changes in brain function following sub-concussive head impacts. And although the magnitude of the acute changes observed was small, it is the presence of the effect that is of interest. This measure was previously shown to be altered in confirmed concussion, but the acute changes in corticomotor inhibition, accompanied by cognitive changes, following the sub-concussive impact of football heading raise concerns that this practice, routine in soccer, may affect brain health.

Funding and Acknowledgements

This work was supported by the National Institute for Health Research (NIHR) Brain Injury Healthcare Technology Cooperative. This work was supported by existing funding awarded to L.W. as part of Framework 7 programme of the European Union (CENTER-TBI, Grant number: 602150-2). The work made use of a TMS coil to which the company Smartfish contributed £1500 for purchase of. T.DiV.'s postgraduate study is support by the research office of Stirling University. W.S. is supported by a NHS Research Scotland Career Researcher Fellowship. D.I.D. and M.I. are members of SINAPSE - see www.sinapse.ac.uk.

The funders had no input in the conception or design of the study, other than NIHR suggesting, at the design stage, to add a full recovery assessment time-point. The funders also had no input in the interpretation or presentation of the results.

Declaration

None of the authors have a competing interest to declare.

Author Contributions

TDV, A.H., L.W., W.S., D.I.D, and M.I. conceived of the study, TDV, A.H., L.W., W.S., S.G., G.H., D.I.D, and M.I. designed the study; TDV executed the study under the guidance of A.H., L.W., S.G., G.H., and M.I.; TDV analyzed data; TDV, A.H., L.W., W.S., S.G., G.H., D.I.D, and M.I. interpreted the results; TDV prepared figures; TDV, A.H. and M.I. drafted manuscript; TDV, A.H., L.W., W.S., S.G., G.H., D.I.D, and M.I. edited and revised manuscript; TDV, A.H., L.W., W.S., S.G., G.H., D.I.D, and M.I. approved final version of manuscript.

References

1. Cantu R.C., Hyman M. Houghton Mifflin Harcourt; Boston: 2012. Concussions and Our Kids: America's Leading Expert on How to Protect Young Athletes and Keep Sports Safe. [Google Scholar]

2. Cicchetti D.V. Guidelines, criteria and rules of thumb for evuating normed and standardized assessment instruments in psychology. Psychol. Assess. 1994;6(4):284-290. [Google Scholar]

3. Patlak M., Joy J.E. Is Soccer Bad for Children's Heads? Summary of the IOM Workshop on Neuropsychological Consequences of Head Impact in Youth Soccer. National Academy Press; Washington DC: 2002. Board on neuroscience and behavioural health. [PubMed] [Google Scholar]

4. Peugh J.L., Enders C.K. Using the SPSS Mixed procedure to fit hierarchical linear and growth trajectory models. Educ. Psychol. Meas. 2005;65:811-835. [Google Scholar]

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# data[].attributes.attachment_link.title
Evidence for Acute Electrophysiological and Cognitive Changes Following Routine Soccer Heading

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There is growing concern around the effects of concussion and sub-concussive impacts in sport. Routine game-play in soccer involves intentional and repeated head impacts through ball heading. Although heading is frequently cited as a risk to brain ...

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Abstract

Introduction

There is growing concern around the effects of concussion and sub-concussive impacts in sport. Routine game-play in soccer involves intentional and repeated head impacts through ball heading. Although heading is frequently cited as a risk to brain health, little data exist regarding the consequences of this activity. This study aims to assess the immediate outcomes of routine football heading using direct and sensitive measures of brain function.

Methods

Nineteen amateur football players (5 females; age 22 ± 3 y) headed machine-projected soccer balls at standardized speeds, modelling routine soccer practice. The primary outcome measure of corticomotor inhibition measured using transcranial magnetic stimulation, was assessed prior to heading and repeated immediately, 24 h, 48 h and 2 weeks post-heading. Secondary outcome measures were cortical excitability, postural control, and cognitive function.

Results

Immediately following heading an increase in corticomotor inhibition was detected; further to these electrophysiological alterations, measurable reduction memory function were also found. These acute changes appear transient, with values normalizing 24 h post-heading.

Discussion

Sub-concussive head impacts routine in soccer heading are associated with immediate, measurable electrophysiological and cognitive impairments. Although these changes in brain function were transient, these effects may signal direct consequences of routine soccer heading on (long-term) brain health which requires further study.

Keywords: Sports concussion, Transcranial magnetic stimulation, Sub-concussion, Traumatic brain injury

Highlights

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Standard soccer heading results in immediate and measurable alterations in brain function.

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Changes in short and long term memory function and corticomotor inhibition are detectable immediately after soccer heading.

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These changes in brain function after just a single session of heading appear transient.

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These data provide direct evidence of immediate brain functional impairment associated with soccer heading.

Questions have been raised over whether soccer heading might have an effect on a player's brain, with particular worry over the proposed link between brain injury and increased risk of dementia. However, until now there have been no studies of the immediate effects of heading in soccer directly on brain function. This study found that just a single session of heading practice resulted in temporary impairment of short and long term memory function and in electrophysiological function of the brain. Whether these effects remain temporary after repeated soccer heading exposure and their long-term consequences on brain health must now be investigated.

1. Introduction

With increased awareness of immediate and late complications of head injuries in sport, in particular the proposed association between exposure to repetitive concussion and late neurodegenerative disease ( Hay et al., 2016), there have been considerable efforts to reduce risk of injury and better manage concussions when they do arise ( McCrory et al., 2013). Soccer (association football) is acknowledged as the most popular participation sport globally, with routine game-play in soccer involving intentional and repeated head impacts through heading the ball; a skill regularly included in training sessions and from a young age. Therefore, although rates of concussion are relative low in soccer compared to other contact sports such as rugby union or American football ( Pfister et al., 2016), participation rates and the incidence of intentional sub-concussive impacts through heading in training and match play are such that the safety of heading in soccer has been questioned in some quarters ( Patlak and Joy, 2002).

Though accepted as part of routine game-play, emerging evidence suggests exposure to repeated sub-concussive impacts in soccer may be associated with measurable changes in brain structure and function, and perhaps with late neurodegenerative disease. Rotational headers may prove of particular interest as they are often performed in training drills and matches (i.e. corner kicks) and are believed to be more injurious compared to linear accelerations ( Cantu and Hyman, 2012). Imaging studies over the course of a season in active soccer players report evidence of white matter microstructural changes with associated impaired cognition ( Lipton et al., 2013). Further, imaging of former professional soccer players aged 40-65 demonstrates evidence of cortical thinning, again with associated cognitive impairment ( Koerte et al., 2015). Regarding longer term outcomes, recent identification of a form of dementia known as chronic traumatic encephalopathy (CTE) in athletes from a range of contact sports (for review see Smith et al., 2013) including soccer ( Geddes et al., 1999, McKee et al., 2014) has drawn attention to the possibility that head impacts in soccer might be associated with increased risk of neurodegenerative disease.

Nevertheless, despite growing evidence on risks from the cumulative effects of sport-related head impacts and anxieties around the safety of ball-heading, little data exists demonstrating direct consequences of heading on brain function. Transcranial magnetic stimulation (TMS) can be used to assess a variety of indices of function in the brain to muscle pathway ( Goodall et al., 2014). Further, TMS has demonstrated utility in quantifying electrophysiological changes in concussion ( Major et al., 2015). The most consistent TMS marker of concussion (both acutely and longitudinally) appears to be corticomotor inhibition ( Major et al., 2015, Pearce et al., 2015, Miller et al., 2014), expressed by a longer period of electromyographic silence (cortical silent period - cSP), after a motor evoked potential (MEP) is delivered to the primary motor cortex during contraction. Given the apparent high sensitivity to identify alterations in brain function, TMS could potentially be used to detect acute changes in brain function following sub-concussive head impacts. The relative novelty of TMS used in this context makes interpretation in terms clinically meaningful effects difficult, but its appeal is sensitivity in detecting direct brain changes ( De Beaumont et al., 2007). It potentially highlights neurochemical changes that can be used to direct routes of investigation into the effects of sub-concussive impacts on the brain. Therefore, the aim was to study the use of TMS corticomotor inhibition in the lower limbs as primary outcome measure to detect acute changes in brain function from repetitive sub-concussive head impacts simulating routine soccer heading. We hypothesized that there would be a (transient) increase in corticomotor inhibition following a standardized bout of soccer heading, which may be accompanied by measurable changes in other established but less sensitive or less objective indexes of changes to brain function and brain injury as secondary outcome measures such as cognitive tests.

2. Methods

2.1. Approvals and Recruitment

The study was approved by the local Research Ethics Committee and procedures conformed to the guidelines set out by the Declaration of Helsinki. Written informed consent was obtained from all participants, prior to taking part. Twenty-three healthy, amateur football players (5 females; age 22 ± 3 y; weight 72.9 ± 8.3 kg; height 175.4 ± 10.2 cm) were recruited for study via advertisement on university noticeboards and meetings with local football clubs. Participants were excluded from taking part if they presented with any of the following: 1) history of brain injury resulting in loss of consciousness; 2) history of a neurological condition; 3) history of concussion in the 12 months prior to taking part; 4) family history of epilepsy; 5) use of psychoactive recreational or prescription drugs. Data from one participant could not be analyzed and three more participants withdrew from the study for personal reasons. The final cohort included a total of nineteen participants.

2.2. Study Design

Participants were asked to refrain from vigorous physical activity, consuming alcohol and caffeine or smoking for 24 h prior to each study session. Furthermore, participants were required to present to the laboratory fasted where they were provided with a standardized breakfast. At the first experimental session baseline measures for cognitive function, postural control, corticospinal excitability and corticomotor inhibition were recorded in this order; assessments thereafter recorded in the same order at each time point during study. Following baseline testing, participants underwent the heading protocol and then repeated the measures at 4 follow-up time points (taking measures in reverse order from the baseline order, starting with the TMS primary outcome measure); immediately post-heading and at 24 h, 48 h and 14 days following the heading protocol. The decision to include the 48 h follow-up was to assess the transient nature of the effects of heading, and the 14 day follow-up was intended as a time point at which complete "wash out" would have occurred following heading impact. Prior to commencement of study data collection participants attended the laboratory for a familiarization session, during which they completed all outcome measures to acquaint them with the assessment procedures and minimize later learning effects.

2.3. Heading Protocol

The heading protocol consisted of heading a standard football (400 g; 70 cm circumference; 8 psi) projected at a speed of 38·7 ± 2.1 kph from a football delivery device (JUGS sports, Tualatin, USA) positioned 6 m from participants, simulating routine soccer game-play ( Haran et al., 2013, Broglio et al., 2004). Participants were instructed to perform a rotational header, redirecting the football perpendicularly to the initial trajectory, with each session consisting of 20 consecutive head impacts over a 10 min period, replicating typical heading practice. A custom-built accelerometer placed at the back of the participant's head recorded linear g-force of the head during impact. Ball speed was determined based on the participants' perceived ability to head the ball with a minimum speed of 30 kph and maximum speed of 50 kph.

2.4. Transcranial Magnetic Stimulation

Motor evoked potentials (MEPs) were elicited in the rectus femoris of the dominant leg via single pulse TMS and assessed using electromyographic (EMG) recordings (see below). Single magnetic stimuli of 1 ms duration where applied over the contralateral primary motor cortex using a magnetic stimulator (Magstim 200 ² unit, The Magstim Company Ltd., Whitland, UK) and a 110 mm double cone coil. Optimal coil location for generating MEPs was determined by placing the coil over the motor cortex, laterally to the vertex; the area where the largest MEP peak-to-peak amplitudes occurred was identified and marked on the scalp with ink ( Goodall et al., 2009). The active motor threshold for the quadriceps femoris was determined by increasing stimulator output from 10% by 5% increments, while the participant held a 10% maximal voluntary contraction (MVC) isometric contraction until discernible MEPs were visible ( Wilson et al., 1995). Once this individual level was established, subsequent stimulations were delivered at 130% of active motor threshold.

MEPs, alongside all other EMG measures, were recorded with participants sitting with their dominant leg secured to a calibrated load cell of an isokinetic dynamometer (Kin-Com, Chattecx Corp, Chattanooga Group Inc., Tennessee). Knee angle was set at 60° (0° being fully extended limb) and the arm of the dynamometer was set such that the axis of rotation was aligned with the participant's lateral femoral condyle.

To assess the primary outcome measure corticomotor inhibition participants were required to perform maximal knee extensor voluntary contractions (MVCs) of 5 s duration while a single TMS stimulation was delivered over the motor cortex. This was repeated three times with a minute's rest between each contraction, as is common practice. Corticomotor inhibition was quantified as the cortical silent period (cSP) duration, taken from the stimulation artefact to the resumption of discernible, uninterrupted EMG activity from the muscle ( Fig. 1). By measuring cSP at MVC, even though this limits the number of repetitions feasible, we ensure to recruit a motor unit pool large enough to show an effect. Measuring cSP at lower intensity may not be as sensitive since a smaller pool of motor units is recruited, reducing the relative effect size of GABA inhibitory mechanisms on the EMG signal. In turn, making the cSP measurements less sensitive in detecting subtle and transient cortico-spinal changes. During the assessment of secondary outcome measure corticospinal excitability, participants maintained a 20% MVC isometric contraction while 20 single TMS pulses, separated by 6 s, were delivered over the motor cortex. Corticospinal excitability was determined as the average MEP amplitude normalized to the maximal response elicited by motor nerve stimulation (%Mmax, see below). We chose to assess cortical excitability and inhibition in the lower limbs rather than in the upper limbs because of its functional relevance; in soccer, changes in lower limb may be more valid as they relate directly to gait and performance.

2.5. Electromyography and Femoral Nerve Stimulation

Electromyographic activity was recorded using a wireless system (Biopac Systems, Inc. Goleta, CA, USA). Data were sampled at 2 kHz, and filtered using 500 Hz low and 1.0 Hz high band filters. Signals were analyzed offline (Acqknowledge, v3.9.1.6, Biopac Systems, Inc. Goleta, CA, USA). EMG activity was assessed using Ag/AgCl surface electrodes (Vermed, Devon, UK) with an intra-electrode distance of 2 cm positioned over rectus femoris; prior to electrode placement, the area of interest was shaved and abraded as per Surface Electromyography for the Non-Invasive Assessment of Muscles (SENIAM) guidelines. The position of each electrode was marked with permanent ink to ensure consistent placement during subsequent visits.

Peripheral stimulation of the femoral motor nerve was administered using an electrical stimulator (Biopac Systems, Inc.). The stimulation site was identified by locating the femoral artery and placing a self-adhesive surface electrode (cathode) lateral to it, high over the femoral triangle, with the anode on the buttock. Single stimuli were delivered to the muscle while participants maintained a 20% MVC isometric contraction, and the intensity of stimulation was increased until a plateau in twitch amplitude and rectus femoris M-wave (Mmax) occurred. Supramaximal stimulation was delivered by increasing the final stimulator output intensity by a further 30%.

2.6. Cognitive Function

Secondary outcome measure cognitive function was assessed in a quiet room using the Cambridge Neuropsychological Test Automated Battery (CANTAB), a computer based cognitive assessment tool and neuropsychological standard. The following CANTAB tasks were included: Reaction Time (RTI; divided attention); Paired Associate Learning (PAL; long-term memory); Spatial Working Memory (SWM; short-term memory); Attention Switching Task (AST; executive function); and Rapid Visual Processing (RVP; sustained attention).

2.7. Postural Control

Secondary outcome measure postural control was assessed using the Biodex Balance System SD (BBS; Biodex Medical Systems, Inc. New York, USA). Participants stood on a circular dynamic platform and average sway score was determined by measuring the degree of tilt on anterior-posterior and medial-lateral axes during three, 20 s trials (using dedicated Biodex software, v1.08, Biodex Inc.).

2.8. Statistical Analysis

Immediate post-heading responses were analyzed using a paired t-test, comparing measures before and immediately after the heading protocol. Recovery was analyzed for individual growth curves using the SPSS MIXED model with the restricted maximum likelihood method in keeping with standards for analysis of longitudinal data ( Singer and Willett, 2003, Peugh and Enders, 2005). To achieve this, individual curves were analyzed to examine change over time. The following time points were included: immediate post, 24 h post, 48 h post, two weeks post. Data was checked for skewness and kurtosis and three cognitive measures (SWM, PAL, and RVP) and the balance variable were normalized using log transformation. The 95% lower and upper confidence intervals (CIs) were also calculated from difference of the mean values. Effect sizes (ES) were calculated for non-transformed differences using Cohen's d formula and were quantified as follows: 0.2 = small; 0.5 = medium; 0.8 = large. Statistical significance was set at p ≤ 0.05. Each measure was separate in relation to the hypotheses and therefore no correction for multiple comparisons was necessary. Data are expressed as means (± standard deviation) unless otherwise stated. The funding source had no input in the study other than suggesting at the design stage to add a full recovery assessment time-point.

3. Results

Overall, each participant performed 20 headers, achieving a mean force of impact of 13.1 ± 1.9 g ( Table 1), with a coefficient of variance of 18%(± 3%).

3.1. Effect of Heading on Corticomotor Inhibition and Corticospinal Excitability

Immediately after ball heading there was a measurable increase in the primary outcome measure cSP within 74% (14 out of 19) of participants ( Fig. 2). The cSP duration increased from 117.8(± 19.8)ms at baseline to 123.1(± 17.6)ms (t₍₁₈₎ = − 2.11, p = 0.049; ES 0.28), representing an average increase of 5.4(± 4.8)% in cSP duration, compatible with increased corticomotor inhibition. This increase in cSP proved transient with apparent normalization to baseline in subsequent follow-up assessments at 24 h, 48 h and 14 days (F(1,18) = 4.23, p = 0.04) ( Fig. 3). There was a moderate, but not significant, relationship between these acute increases in cSP and g-force on impact with the ball ( r = 0.37, p = 0.07 one-tailed).

To determine the reproducibility of the primary outcome measure the intraclass correlation coefficient (ICC) was calculated between the baseline and the 2 weeks post-measure. ICC for the two measures was 0.764, suggesting excellent agreement ( Cicchetti, 1994). Furthermore, no within-participant differences were found between the two time points using a paired t-test (t₍₁₈₎ = − 0.47, p < 0.63; ES 0.09; CI − 10.36 to 6.53).

No changes were found on the secondary TMS outcome measure corticospinal excitability; MEP amplitude demonstrated no change in the acute phase immediately after ball heading, nor in the follow-up assessment time-points ( Table 2). There was no notable change in knee extensor MVC after heading the ball ( Table 2), suggesting the participants did not experience significant muscular fatigue that might interfere with TMS measurement.

3.2. Altered Cognitive Function Following Heading

Immediately after the heading protocol there was a reduced performance compared to baseline in two CANTAB sub-tasks assessing accuracy on different aspects of memory. Specifically, Spatial Working Memory (SWM) error scores were significantly higher (t₍₁₈₎ = − 2.28, p = 0.03, ES 0.3) immediately after the heading protocol, compatible with impairment in short-term memory ( Fig. 4a). Furthermore, total adjusted error score on the Paired Associated Learning (PAL) task immediately after heading increased by 67% (t₍₁₈₎ = − 3.05, p = 0.007, ES 0.5), compatible with a reduced long-term memory function ( Fig. 4b). These disturbances in short- and long-term memory proved transient, with normalization to baseline performance in SWM (F(1,18) = 10.28, p = 0.002) and PAL (F(1,18) = 11.14, p = 0.002) in the subsequent follow-up assessments at 24 h, 48 h and 14 days ( Table 2).

Heading only significantly affected memory function; the remaining CANTAB tasks assessing aspects of attention and processing speed did not show significant heading-associated decrements compared to baseline assessments ( Table 2). No change was detected on the Rapid Visual Processing task, with RVP A′ scores close to ceiling/maximum, making the measure insensitive to change. There was a marginal improvement on the median corrected latency scores of the executive function Attention Shifting Task (t₍₁₈₎ = 2.52, p = 0.021), possibly due to practice. On the Choice RTI measure there was no effect of heading on decision times (t₍₁₈₎ = 0.69, p = 0.5) ( Table 2).

4. Discussion

Following a standardized session of football heading designed to simulate routine soccer practice our data demonstrate immediate alterations in brain electrophysiological and cognitive function compared to baseline assessments in a cohort of healthy, young soccer players. Specifically, using TMS we found a measurable increase in cortical silent period (cSP) after just 20 consecutive headers. Furthermore, in cognitive assessments, our data demonstrate evidence of decreases in measures of both short- and long-term memory immediately following heading. Notably, in this single exposure paradigm, these alterations in brain corticomotor inhibition and cognitive function appeared short-lived; the effects apparently normalizing in follow-up assessments from 24 h onwards. In contrast to previous studies in athletes and patients with confirmed concussion or mild TBI ( De Beaumont et al., 2007, Chistyakov et al., 2001, Bernabeu et al., 2009, Livingston et al., 2010) these novel observations demonstrate, for the first time, detectable alterations in brain function in footballers exposed to 'routine' head impacts not associated with clinically recognizable brain injury.

The prolonged silent period of neuromuscular recruitment found in this study is a sign of increased inhibition in the motor system and is thought to reflect GABA activity ( Inghilleri et al., 1993, McDonnell et al., 2006) which is the most powerful inhibitor in the motor system. Although the mechanisms behind corticomotor inhibition are not fully understood ( Chen et al., 1999), increased inhibition following repeated sub-concussive head impact may reflect protective mechanisms against minor injury. What is a concern however is that such protective mechanisms could become maladaptive when stimulated repeatedly, as occurs during soccer heading practice. Albeit apparently transient, the acute increases in corticomotor inhibition following football heading could trigger a pathological process damaging brain health through the accumulative effect of sub-concussive head impact. Increased corticomotor inhibition silent period has been found to be associated with pathophysiology in brain damage suggesting a link between functional deficits and hyperactivity of cortical inhibitory interneurons ( Classen et al., 1997). Further study into the dynamic metabolic processes as a direct result of soccer heading is required. When we understand the complex interplay between functional, metabolic, and structural brain changes following repeated sub-concussive head impact, we can establish the link to accumulative and long-term consequences. At present, the current findings at least suggest acute brain changes occur as a direct consequence of soccer heading.

As well as increased corticomotor inhibition, parameters of memory function were altered following the heading protocol, consistent with a recent report of a relationship between memory function and history of heading in soccer ( Lipton et al., 2013). Furthermore, a study of retired Australian Rules footballers found that elite players performed more poorly on the Paired Associate Learning test than amateurs ( Pearce et al., 2014). Practical limitations of cognitive-based tests to detect impairment in athletes are due to reliability: in high performance sports athletes have been recognized to purposely produce low baseline performances on cognitive tests to allow them to avoid removal from play, or to reduce return to play intervals ( Erdal, 2012).

For completeness postural control (balance) was included as a secondary, albeit indirect, outcome measure as concussion has been shown to result in impaired balance ( McCrory et al., 2013, Powers et al., 2014), yet the participants in the current study were able to maintain their balance despite an increased level of corticomotor inhibition. And while one study has shown a decrease in postural control following bouts of soccer heading ( Haran et al., 2013), another study has not ( Broglio et al., 2004); and now our own show no change in postural control.

Secondary TMS outcome measure cortical excitability has previously been shown to decrease following TBI ( De Beaumont et al., 2007, Chistyakov et al., 2001, Bernabeu et al., 2009, Livingston et al., 2010), yet we demonstrated no such change following ball heading. The reason why changes were seen in cortical inhibition and not cortical excitability may be due to the different levels of muscle contractile force applied during recording of the two parameters (20% MVC for excitability vs. 100% MVC for inhibition, see the introduction for its justification). Furthermore, it should be noted that measuring cortical excitability is a less straightforward procedure than corticomotor inhibition as it requires MEP normalization to maximal motor nerve response ( Goodall et al., 2009). Primary outcome measure TMS corticomotor inhibition was thought to be most sensitive to quantifying electrophysiological changes based on a recent systematic review ( Major et al., 2015), and is a direct measure of changes to brain function.

Future work should include a control activity, such as body movement without head impact. However, the current pattern of results leaves little doubt that the changes in brain function were related to head impact rather than physical activity. The force of maximal knee contraction was not reduced after heading, therefore the absence of a physical exercise control group it is highly unlikely to explain the effect on corticomotor inhibition or memory function. Nevertheless, a future extension of this work can focus on the acute effects of heading now that the transience of the effect has been established, and would be well placed to reveal the mechanisms underlying these brain changes through a cross-over design that includes a control activity. Furthermore, because it is likely that sub-concussive impacts are more general in nature (i.e. they do not affect single muscles) future work should assess corticomotor inhibition in a larger number of muscles, possibly encompassing both upper and lower limbs. Further study into the dynamic metabolic processes as a direct result of soccer heading is required. Implementing the use of magnetic resonance spectroscopy in future studies could help determine short-term alterations in GABA and glutamate responses. With regard to changes in GABA, because of the use of single-pulse TMS in this study, we were only able to report on the activity of GABA B, while the use of paired-pulse TMS in future work can distinguish modulation of GABA A and GABA B. Critically, however, the sensitivity of the current primary outcome measure suggests that corticomotor inhibition through future dose-response studies has the potential to provide the evidence-base to guide safe engagement in contact-sports, such as soccer.

5. Conclusion

The current study is the first to show direct evidence for acute changes to corticomotor function and changes to memory function following routine soccer heading. It is furthermore the first study to show that corticomotor inhibition, measured by TMS, is able to detect acute transient changes in brain function following sub-concussive head impacts. And although the magnitude of the acute changes observed was small, it is the presence of the effect that is of interest. This measure was previously shown to be altered in confirmed concussion, but the acute changes in corticomotor inhibition, accompanied by cognitive changes, following the sub-concussive impact of football heading raise concerns that this practice, routine in soccer, may affect brain health.

Funding and Acknowledgements

This work was supported by the National Institute for Health Research (NIHR) Brain Injury Healthcare Technology Cooperative. This work was supported by existing funding awarded to L.W. as part of Framework 7 programme of the European Union (CENTER-TBI, Grant number: 602150-2). The work made use of a TMS coil to which the company Smartfish contributed £1500 for purchase of. T.DiV.'s postgraduate study is support by the research office of Stirling University. W.S. is supported by a NHS Research Scotland Career Researcher Fellowship. D.I.D. and M.I. are members of SINAPSE - see www.sinapse.ac.uk.

The funders had no input in the conception or design of the study, other than NIHR suggesting, at the design stage, to add a full recovery assessment time-point. The funders also had no input in the interpretation or presentation of the results.

Declaration

None of the authors have a competing interest to declare.

Author Contributions

TDV, A.H., L.W., W.S., D.I.D, and M.I. conceived of the study, TDV, A.H., L.W., W.S., S.G., G.H., D.I.D, and M.I. designed the study; TDV executed the study under the guidance of A.H., L.W., S.G., G.H., and M.I.; TDV analyzed data; TDV, A.H., L.W., W.S., S.G., G.H., D.I.D, and M.I. interpreted the results; TDV prepared figures; TDV, A.H. and M.I. drafted manuscript; TDV, A.H., L.W., W.S., S.G., G.H., D.I.D, and M.I. edited and revised manuscript; TDV, A.H., L.W., W.S., S.G., G.H., D.I.D, and M.I. approved final version of manuscript.

References

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# data[].attributes.attachment_link.title
Evidence for Acute Electrophysiological and Cognitive Changes Following Routine Soccer Heading

# data[].attributes.attachment_link.description
There is growing concern around the effects of concussion and sub-concussive impacts in sport. Routine game-play in soccer involves intentional and repeated head impacts through ball heading. Although heading is frequently cited as a risk to brain ...

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The effect of visual and sensory performance on head impact biomechanics in college football players - PubMed

# data[].attributes.attachment_link.description
The development of prevention strategies is critical to address the rising prevalence of sport-related concussions. Visual and sensory performance may influence an individual’s ability to interpret environmental cues, anticipate opponents’ actions, and create appropriate motor responses limiting the …

# data[].attributes.attachment_link.title
The Effect of Visual and Sensory Performance on Head Impact Biomechanics in College Football Players - Annals of Biomedical Engineering

# data[].attributes.attachment_link.description
The development of prevention strategies is critical to address the rising prevalence of sport-related concussions. Visual and sensory performance may influence an individual’s ability to interpret environmental cues, anticipate opponents’ actions, and create appropriate motor responses limiting the severity of an impending head impact. The purpose of this study was to determine the relationship between traditional and visual sensory reaction time measures, and the association between visual and sensory performance and head impact severity in college football players. Thirty-eight collegiate football players participated in the study. We used real-time data collection instrumentation to record head impact biomechanics during games and practices. Our findings reveal no significant correlations between reaction time on traditional and visual sensory measures. We found a significant association between head impact severity and level of visual and sensory performance for multiple assessments, with low visual and sensory performers sustaining a higher number of severe head impacts. Our findings reveal a link between level of visual and sensory performance and head impact biomechanics. Future research will allow clinicians to have the most appropriate testing batteries to identify at-risk athletes and create interventions to decrease their risk of injurious head impacts.

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Effects of Soccer Heading on Brain Structure and Function

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Soccer is the most popular sport in the world, with more than 265 million players worldwide, including professional and amateur ones. Soccer is unique in comparison to other sports, as it is the only sport in which participants purposely use their…

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Incorporate more microsaccade literature into this plan.